Sox2-dependent maintenance of mouse oligodendroglioma involves the Sox2-mediated downregulation of Cdkn2b, Ebf1, Zfp423, and Hey2

Glia. 2021 Mar;69(3):579-593. doi: 10.1002/glia.23914. Epub 2020 Sep 25.

Abstract

Cancer stem cells (CSC) are essential for tumorigenesis. The transcription factor Sox2 is overexpressed in brain gliomas, and is essential to maintain CSC. In mouse high-grade glioma pHGG cells in culture, Sox2 deletion causes cell proliferation arrest and inability to reform tumors after transplantation in vivo; in Sox2-deleted cells, 134 genes are derepressed. To identify genes mediating Sox2 deletion effects, we overexpressed into pHGG cells nine among the most derepressed genes, and identified four genes, Ebf1, Hey2, Zfp423, and Cdkn2b, that strongly reduced cell proliferation in vitro and brain tumorigenesis in vivo. CRISPR/Cas9 mutagenesis of each gene, individually or in combination (Ebf1 + Cdkn2b), significantly antagonized the proliferation arrest caused by Sox2 deletion. The same genes also repressed clonogenicity in primary human glioblastoma-derived CSC-like lines. These experiments identify a network of critical tumor suppressive Sox2-targets whose inhibition by Sox2 is involved in glioma CSC maintenance, defining new potential therapeutic targets.

Keywords: Sox2; cancer stem cells; gene regulatory networks; human glioblastoma; mouse oligodendroglioma; transcription factors; tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors
  • Brain Neoplasms* / genetics
  • Carcinogenesis / genetics
  • Cell Line, Tumor
  • Down-Regulation
  • Glioblastoma*
  • Glioma* / genetics
  • Mice
  • Neoplastic Stem Cells / metabolism
  • Oligodendroglioma*
  • Repressor Proteins
  • SOXB1 Transcription Factors / genetics
  • SOXB1 Transcription Factors / metabolism
  • Trans-Activators

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Ebf1 protein, mouse
  • Hey2 protein, mouse
  • Repressor Proteins
  • SOXB1 Transcription Factors
  • Trans-Activators